氮添加促进丛枝菌根真菌和根系协作维持土壤磷有效性

doi:10.17521/cjpe.2021.0280

植物生态学报 ›› 2022, Vol. 46 ›› Issue (7): 811-822.DOI: 10.17521/cjpe.2021.0280

所属专题：根系生态学；菌根真菌；微生物生态学

氮添加促进丛枝菌根真菌和根系协作维持土壤磷有效性

谢欢¹, 张秋芳², 陈廷廷¹, 曾泉鑫¹, 周嘉聪¹, 吴玥¹, 林惠瑛¹, 刘苑苑¹, 尹云锋¹, 陈岳民¹^,^*()

¹福建师范大学地理科学学院, 湿润亚热带山地生态国家重点实验室培育基地, 福州 350007
²北京大学城市与环境学院, 北京 100871

收稿日期:2021-08-02 接受日期:2021-12-09 出版日期:2022-07-20 发布日期:2022-01-07
通讯作者: 陈岳民
作者简介:* (ymchen@fjnu.edu.cn)
基金资助:
福建省自然科学基金(2020J01142)

Interaction of soil arbuscular mycorrhizal fungi and plant roots acts on maintaining soil phosphorus availability under nitrogen addition

XIE Huan¹, ZHANG Qiu-Fang², CHEN Ting-Ting¹, ZENG Quan-Xin¹, ZHOU Jia-Cong¹, WU Yue¹, LIN Hui-Ying¹, LIU Yuan-Yuan¹, YIN Yun-Feng¹, CHEN Yue-Min¹^,^*()

¹State Key Laboratory of Subtropical Mountain Ecology, School of Geographical Science, Fujian Normal University, Fuzhou 350007, China
²College of Urban and Environmental Sciences, Peking University, Beijing 100871, China

Received:2021-08-02 Accepted:2021-12-09 Online:2022-07-20 Published:2022-01-07
Contact: CHEN Yue-Min
Supported by:
Natural Science Foundation of Fujian Province(2020J01142)

摘要/Abstract

摘要：

磷是亚热带地区植物生长的主要限制营养元素, 而氮沉降量的增加会降低土壤磷的有效性。该研究以微生物和植物细根为重点探究土壤磷转化, 揭示氮沉降背景下低磷有效性土壤的磷供应及生产力维持。通过在福州长安山模拟氮沉降实验, 设置对照(0 kg·hm^-2·a^-1)、低氮(40 kg·hm^-2·a^-1)和高氮(80 kg·hm^-2·a^-1) 3个处理, 收集杉木(Cunninghamia lanceolata)幼苗的土壤和根系样本, 综合分析土壤磷组分和养分含量、土壤微生物特征和植物根系特征。结果显示, 与对照处理相比, 低氮处理显著增加土壤易分解态有机磷、中等易分解态无机磷和闭蓄态磷含量, 但是显著降低原生矿物态磷和中等易分解态有机磷含量; 而高氮处理对土壤磷组分无显著影响。冗余分析表明, 土壤酸性磷酸酶活性、丛枝菌根真菌的相对丰度、土壤微生物生物量磷含量和根系生物量是解释土壤磷组分变化的重要微生物和植物因子。方差分解分析发现植物根系特征-土壤微生物特征共同解释了土壤磷组分变化的57%, 并且通过相关分析发现丛枝菌根真菌的相对丰度和根系生物量呈显著正相关关系。综上所述, 低水平的氮输入促进土壤丛枝菌根真菌的定殖, 丛枝菌根真菌和杉木根系通过协作促进中等易分解态有机磷和原生矿物态磷向易分解态磷的转换, 维持了杉木幼苗的生长。

关键词: 氮添加, 磷, 微生物特征, 根系特征, 杉木, 幼苗

Abstract:

Aims Phosphorus is one of the major limiting nutrients for plant growth in subtropical areas, whereas increasing nitrogen deposition may be a limiting factor in determining the availability of soil phosphorus. Here, focusing on soil microorganisms and plant fine roots, we explored the transformation of soil phosphorus to unravel the maintenance of soil phosphorus supply and plant productivity with low availability under nitrogen deposition.

Methods At the Fuzhou Changʼan Mountain in Fujian Province, China, control (0 kg·hm^-2·a^-1), low nitrogen (40 kg·hm^-2·a^-1), and high nitrogen (80 kg·hm^-2·a^-1) treatments were set up to simulate nitrogen addition. Soil and root samples of Cunninghamia lanceolata seedlings were then collected to comprehensively analyze soil phosphorus and nutrient contents as well as microbiological-plant root characteristics.

Important findings The results showed that the contents of soil labile organic phosphorus, moderately labile inorganic phosphorus and occluded phosphorus were significantly increased, whereas those of primary mineral phosphorus and moderately labile organic phosphorus decreased under the low nitrogen treatment as compared to the control treatment. However, there were no significant changes under the high nitrogen treatment. Redundancy analysis indicated that soil acid phosphatase activity, relative abundance of mycorrhizal fungi, soil microbial biomass phosphorus content, and root biomass were important soil microbiological-plant root characteristics factors that could explain the changes in soil phosphorus components. Variance partitioning analysis revealed that the soil microbiological-plant root characteristics synergy explained 57% of the alternations in soil phosphorus components, whereas correlation analysis showed a significant positive correlation between the relative abundance of mycorrhizal fungi and root biomass. Overall, these results suggest that mycorrhizal colonization is promoted under a low level of nitrogen input and the synergistic action of mycorrhizal fungi and C. lanceolata fine roots promotes the conversion of moderately labile organic and primary mineral phosphorus to labile phosphorus, thus maintaining the growth of C. lanceolata seedlings.

Key words: nitrogen addition, phosphorus, microbiologic characteristic, root characteristic, Cunninghamia lanceolata, seedling

谢欢, 张秋芳, 陈廷廷, 曾泉鑫, 周嘉聪, 吴玥, 林惠瑛, 刘苑苑, 尹云锋, 陈岳民. 氮添加促进丛枝菌根真菌和根系协作维持土壤磷有效性. 植物生态学报, 2022, 46(7): 811-822. DOI: 10.17521/cjpe.2021.0280

XIE Huan, ZHANG Qiu-Fang, CHEN Ting-Ting, ZENG Quan-Xin, ZHOU Jia-Cong, WU Yue, LIN Hui-Ying, LIU Yuan-Yuan, YIN Yun-Feng, CHEN Yue-Min. Interaction of soil arbuscular mycorrhizal fungi and plant roots acts on maintaining soil phosphorus availability under nitrogen addition. Chinese Journal of Plant Ecology, 2022, 46(7): 811-822. DOI: 10.17521/cjpe.2021.0280

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2021.0280

https://www.plant-ecology.com/CN/Y2022/V46/I7/811

图/表 11

图1 土壤磷(P)组分的提取流程和分类(图片内容参考自Hedley等(1982), Tiessen和Moir (2007))。

Fig. 1 Extraction procedure and classification of soil phosphorus (P) fractions (Picture content referenced from Hedley et al. (1982), Tiessen & Moir (2007)). Pi, inorganic phosphorus; Po, organic phosphorus.

表1 施氮对福州长安山土壤理化性质的影响

Table 1 Effects of nitrogen (N) addition on soil physical and chemical properties at the Fuzhou Changʼan Mountain in Fujian Province

处理 Treatment	pH	总碳含量 Total carbon (C) content (g·kg^-1)	总氮含量 Total N content (g·kg^-1)	有效氮含量 Available N content (mg·kg^-1)	可溶性有机碳含量 Dissolved organic C content (mg·kg^-1)	可溶性有机氮含量 Dissolved organic N content (mg·kg^-1)
CK	4.55 ± 0.06^a	16.30 ± 0.23^a	1.47 ± 0.03^a	7.97 ± 0.22^b	7.67 ± 0.60^a	4.61 ± 0.40^b
LN	4.51 ± 0.06^a	16.20 ± 0.04^a	1.48 ± 0.05^a	8.58 ± 0.49^a	6.78 ± 0.44^b	6.68 ± 0.36^a
HN	4.40 ± 0.09^b	16.61 ± 0.24^a	1.50 ± 0.02^a	8.83 ± 0.25^a	3.99 ± 0.71^c	7.24 ± 0.71^a
p	0.03	0.06	0.57	0.01	<0.01	<0.01

图2 施氮(N)对福州长安山土壤磷(P)组分含量的影响(平均值±标准差)。不同小写字母表示处理间差异显著(p < 0.05)。CK, 对照; HN, 高氮; LN, 低氮。

Fig. 2 Effects of nitrogen (N) addition on soil phosphorus (P) components contents at the Fuzhou Changʼan Mountain in Fujian Province (mean ± SD). Different lowercase letters mean significant difference among different treatments (p < 0.05). CK, control; HN, high nitrogen; LN, low nitrogen. Pi, inorganic phosphorus; Po, organic phosphorus.

表2 施氮(N)对福州长安山土壤真菌群落的影响(%)(平均值±标准差)

Table 2 Effects of nitrogen addition on soil fungi community (%) at the Fuzhou Changʼan Mountain in Fujian Province (mean ± SD)

处理 Treatment	子囊菌门 Ascomycota	担子菌门 Basidiomycotaota	被孢菌门 Mortierellomycota	未定义 Unclassified	罗兹菌门 Rozellomycota	球囊菌门 Glomeromycota	其他 Other
CK	38.73 ± 9.28^a	26.04 ± 7.02^a	11.94 ± 3.16^a	11.18 ± 1.03^a	9.87 ± 6.22^a	0.27 ± 0.01^b	1.97 ± 0.56^a
LN	39.02 ± 6.00^a	26.16 ± 3.33^a	16.86 ± 3.52^a	10.83 ± 4.13^a	4.61 ± 0.97^a	1.09 ± 0.11^a	1.43 ± 0.48^a
HN	35.05 ± 12.21^a	37.24 ± 13.12^a	14.43 ± 2.39^a	8.11 ± 3.91^a	3.77 ± 1.27^a	0.62 ± 0.01^a	0.90 ± 0.63^a
p	0.809	0.175	0.129	0.400	0.091	<0.001	0.072

表3 施氮对福州长安山土壤酶活性和微生物生物量养分含量的影响(平均值±标准差)

Table 3 Effects of nitrogen (N) addition on soil enzymes activity and microbial biomass nutrient content at the Fuzhou Changʼan Mountain in Fujian Province (mean ± SD)

处理 Treatment	酸性磷酸单酯酶 Acid phosphomonoesterase (nmol·g^-1·h^-1)	酸性磷酸双酯酶 Acid phosphodiesterase (nmol·g^-1·h^-1)	微生物生物量碳含量 Microbial biomass carbon content (mg·kg^-1)	微生物生物量氮含量 Microbial biomass N content (mg·kg^-1)	微生物生物量磷含量 Microbial biomass phosphorus content (mg·kg^-1)
CK	24.68 ± 2.44^b	1.67 ± 0.08^a	215.42 ± 21.87^c	29.59 ± 1.40^a	41.07 ± 3.31^a
LN	48.89 ± 4.08^a	1.72 ± 0.05^a	273.59 ± 18.53^b	26.45 ± 0.98^b	21.75 ± 2.09^b
HN	19.59 ± 2.90^c	1.19 ± 0.03^b	358.27 ± 20.05^a	27.62 ± 0.95^b	20.78 ± 6.45^b
p	<0.001	<0.001	<0.001	0.003	<0.001

表4 施氮对福州长安山植物根系特征的影响(平均值±标准差)

Table 4 Effects of nitrogen (N) addition on plant roots traits at the Fuzhou Changʼan Mountain in Fujian Province (mean ± SD)

处理 Treatment	根系生物量 Root biomass (g·plant^-1)	根系总碳含量 Root total carbon content (g·kg^-1)	根系总氮含量 Root total N content (g·kg^-1)	根系总磷含量 Root total phosphorous content (g·kg^-1)	侵染率 Root colonization rate (%)	直径 root diameter (mm)	比根长 Specific root length (m·g^-1)	比表面积 Specific root surface area (cm·g^-1)	组织密度 Root tissue density (g·cm^-3)
CK	2.79 ± 0.46^b	459.61 ± 4.62^b	9.61 ± 1.20^a	1.66 ± 0.23^a	58.23 ± 8.71^c	0.82 ± 0.13^a	36.13 ± 6.39^a	554.02 ± 25.53^a	0.20 ± 0.10^a
LN	4.01 ± 0.39^a	467.72 ± 8.98^a	10.01 ± 0.98^a	1.37 ± 0.19^ab	80.09 ± 4.13^b	0.69 ± 0.44^a	35.36 ± 9.58^a	265.01 ± 62.72^b	0.62 ± 0.37^a
HN	3.06 ± 0.49^b	470.08 ± 5.63^a	8.63 ± 1.18^a	1.31 ± 0.11^b	89.67 ± 4.69^a	0.39 ± 0.12^a	36.68 ± 12.59^a	342.53 ± 63.65^b	0.44 ± 0.21^a
p	0.003	<0.001	0.180	0.023	<0.001	0.079	0.978	<0.001	0.062

图3 生物因子和非生物因子解释土壤磷组分变化的百分比。

Fig. 3 Percentages of the variance in soil phosphorus components explained by biotic factors and abiotic factors.

图4 土壤微生物特征(A)和植物根系特征(B)对福州长安山土壤磷(P)组分影响的冗余分析(RDA)。

Fig. 4 Redundancy analysis (RDA) of soil microbial (A) and plant roots characteristics (B) on soil phosphorus (P) components at the Fuzhou Changʼan Mountain in Fujian Province. AcP, acid phosphomonolase; AMF, arbuscular mycorrhizal fungi; FRD, fine root diameter; MBC, microbial biomass carbon; MBN, microbial biomass nitrogen; MBP, microbial biomass phosphorus; PD, acid phosphodiesterase; Pi, inorganic phosphorus; Po, organic phosphorus; RC, root colonization; RM, root biomass; RTC, root total carbon; RTD, special root density; RTN, root total nitrogen; RTP, root total phosphorous; SRA, special root area; SRL, special root length.

图5 方差分解分析显示由植物变量和微生物变量解释土壤磷组分变异百分比。

Fig. 5 Variation-partitioning analysis showing the percentages of the variance in soil phosphorus components explained by plant and microorganism variables.

表5 福州长安山土壤微生物特征和植物根系特征的相关系数

Table 5 Correlation coefficients between soil microbial and plant roots characteristics at the Fuzhou Changʼan Mountain in Fujian Province

	根系生物量 Root biomass	直径 Root diameter	比根长 Specific root length	比表面积 Specific root surface area	组织密度 Root tissue density	侵染率 Root colonization rate	根系总碳含量 Root total carbon content
酸性磷酸单酯酶活性 Acid phosphomonoesterase activity	0.713^**	0.264	-0.009	-0.287	-0.434	0.064	0.267
酸性磷酸双酯酶活性 Acid phosphodiesterase activity	0.306	0.541^*	0.001	0.400	-0.585^*	-0.590^*	-0.417
丛枝菌根真菌相对丰度 Mycorrhizal Fungi relative abundance	0.789^**	0.013	0.032	-0.668^**	-0.112	0.485	0.625^*
微生物生物量碳含量 Microbial biomass carbon content	0.007	-0.639^*	-0.042	-0.713^**	0.537^*	0.740^**	0.796^**
微生物生物量氮含量 Microbial biomass nitrogen content	-0.566^*	0.061	-0.068	0.687^**	0.041	-0.589^*	-0.642^**
微生物生物量磷含量 Microbial biomass phosphorus content	-0.439	0.362	0.119	0.829^**	-0.177	0.855^**	-0.894^**

图6 土壤磷(P)组分对施氮(N)的响应概念图。“ ”、“ ”、“ ”分别表示土壤微生物、植物根系指标含量显著增加、降低和无显著变化。“ ”和“ ”分别表示土壤各P组分显著增加和降低。Pi, 无机P; Po, 有机P。

Fig. 6 A conceptual diagram of the responses of soil phosphorus (P) components to nitrogen (N) addition and the regulation effect of soil microbes and plant root systems. “ ”、“ ”、“ ” represent that the contents of soil microbial and plant root index show significant increase, decrease, and no significant change, respectively. “ ” and “ ” represent that soil phosphorus components show significant increase and decrease, respectively. Pi, inorganic phosphorus; Po, organic phosphorus.

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氮添加促进丛枝菌根真菌和根系协作维持土壤磷有效性

Interaction of soil arbuscular mycorrhizal fungi and plant roots acts on maintaining soil phosphorus availability under nitrogen addition

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